Neural interfaces and other advanced technology for stroke recovery

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Restore function after injury Dual Outcome Goals Directly re-animate limb function after severe injury Promote plasticity & sustained

1 Neural interfaces and other advanced technology for stroke recovery Chet Moritz, Ph.D. Associate Professor Rehabilitation Medicine, Physiology & Biophysics Deputy Director Center for Sensorimotor Neural Engineering Goal: Restore function after injury Dual Outcome Goals Directly re-animate limb function after severe injury Promote plasticity & sustained recovery after less severe injury Our Approach: develop a brain-controlled spinal interface (BCSI) to restore limb function after paralysis due to brain or spinal injury (c) Chet Moritz

2 Three approaches to restore function after brain or spinal injury 1. Brain Computer Interfaces (BCI) for Muscle Stimulation 2. Spinal Stimulation for Re-animation 3. Spinal Stimulation for Rehabilitation Brain control of muscle stimulation Control signals recorded from motor cortex...trigger functional electrical stimulation (FES) delivered to paralyzed muscles Katie Ris-Vicari News & Views on Moritz et al; S. Scott, Nature Neuroscience 2008 (c) Chet Moritz

Brain recording methods Signals recorded from outside or

et al Humans control cursors & robot s choices

cursors and robotic hand Intracortical electrodes Ojeman,

robotic arms & hands Donoghue, Schwartz, Nicholalis,

3 Brain recording methods Signals recorded from outside or inside the brain Scalp based EEG Wolpaw, Birbaumer, Rao, et al Humans control cursors & robot s choices Electrocorticography (ECoG) Epilepsy patients control 2D cursors and robotic hand Intracortical electrodes Ojeman, Birbaumer, et al Monkeys & humans control cursors, robotic arms & hands Donoghue, Schwartz, Nicholalis, Shenoy, et al Brain cell activity during wrist movement (c) Chet Moritz

4 Brain cell directional tuning Low-Rate Target High-Rate Target Visual feedback of cell rate with targets oriented in preferred direction Monkey controls cursor with brain cell (c) Chet Moritz

Decoding arm & digit movement intention Hochberg et al

2012 Connecting cortical neurons to control muscle

Neurotrauma 2004 Reanimate limbs using muscle stimulation

5 Decoding arm & digit movement intention Hochberg et al Donoghue, Nature 2012 Collinger et al Schwartz, Lancet 2012 Connecting cortical neurons to control muscle stimulation Extract control signals from brain Anderson, J Neurotrauma 2004 Reanimate limbs using muscle stimulation (FES) FreeHand Peckham et al. J Hand Surgery 2002 (c) Chet Moritz

Brain-controlled muscle stimulation Cell activity directly converted to muscle stimulation (FES) Wrist muscles temporarily paralyzed by nerve block Moritz, Perlmutter & Fetz Nature 2008 Cortical

6 Brain-controlled muscle stimulation Cell activity directly converted to muscle stimulation (FES) Wrist muscles temporarily paralyzed by nerve block Moritz, Perlmutter & Fetz Nature 2008 Cortical control of muscle stimulation Cortical neurons move cursors on computer screen Cortical neurons trigger FES of paralyzed muscles via standard or miniature computer Moritz, Perlmutter & Fetz Nature 2008 (c) Chet Moritz

Brain-control of muscle stimulation Stimulator on Monkeys match 5

torque can be produced without stimulator Moritz, Perlmutter & Fetz

man with SCI 4 years post diving accident Utah/Blackrock Array in M1

7 Brain-control of muscle stimulation Stimulator on Monkeys match 5 levels of wrist torque using cortically-controlled FES Only 5-10% of torque can be produced without stimulator Moritz, Perlmutter & Fetz Nature 2008 Subject using BCI to control muscle FES 23 y/o tetraplegia man with SCI 4 years post diving accident Utah/Blackrock Array in M1 Surface FES array on forearm Bouton et al., Rezai, Nature 2016 (c) Chet Moritz

8 Subject using BCI to control muscle FES Bouton et al., Rezai, Nature 2016 Cell tuning does not predict control of FES Before practice After practice Tuned neurons initially control cursor faster The brain learns to use all neurons equally well to control FES with practice This practice triples the population of useful neurons Moritz, Perlmutter & Fetz Nature 2008 (c) Chet Moritz

Can other cortical areas be used to control FES?

somatosensory cortex can be controlled equally well Moritz & Fetz, J Neural Engineering 2011

cortex contralateral to injury) Can one hemisphere control both hands?

(unaffected) hand A proxy for eventual reanimation of paralyzed hand using FES BCI via

9 Can other cortical areas be used to control FES? Electrodes in spared cortex Area of ischemia Clot in middle cerebral artery Neurons in somatosensory cortex can be controlled equally well Moritz & Fetz, J Neural Engineering 2011 MCA stroke arm paresis Record from spared cortex for control? (e.g. cortex contralateral to injury) Can one hemisphere control both hands? Challenge subjects to Control BCI using ipsilateral cortex Simultaneously control contralateral (unaffected) hand A proxy for eventual reanimation of paralyzed hand using FES BCI via ipsilateral cortex Select directionally-tuned or untuned cells if brain must dissociate ongoing movements from BCI control? Milovanovic, Robinson, Fetz & Moritz, Brain Computer Interface 2015 (c) Chet Moritz

Tuned neurons are less efficient when activity

Fetz & Moritz, Brain Computer Interface 2015

$over right peri-infract cortex Simultaneous$ right BCI & right (unaffected) hand movement

10 Tuned neurons are less efficient when activity must be dissociated Milovanovic, Robinson, Fetz & Moritz, Brain Computer Interface 2015 Stroke survivor using BCI & unaffected hand Right perinatal MCA infarct ECoG electrodes over right peri-infract cortex Simultaneous right BCI & right (unaffected) hand movement Sarma, Ojemann & Rao, in preparation (c) Chet Moritz

11 Decoding digit movement from ECoG ECoG Microgrid Ojemann & Rao Group, PNAS 2010; PNAS 2013; in preparation Micro-ECoG varies with hand grip Ojemann & Rao Groups, in preparation (c) Chet Moritz

12 Synergy-based ECoG control of simulated hand Wu, Ojemann, Rao & Todorov Groups, in preparation Three approaches to restore limb function after CNS injury 1. Brain Controlled Interfaces (BCI) for Muscle Stimulation 2. Spinal Stimulation for Re-animation (c) Chet Moritz

Recruitment of motor units: Size principle Motor units typically recruited from small (S) to large (FF) But FES recruits in Inverse order: large (FF) to small (S) Motor

Advantages of spinal stimulation More natural recruitment order of motor units (Mushahwar & Horsch, 2000) Smooth grading of force Fatigue-resistant contractions Elicit

13 Recruitment of motor units: Size principle Motor units typically recruited from small (S) to large (FF) But FES recruits in Inverse order: large (FF) to small (S) Motor Unit Pool (%) Lieber Skeletal Muscle Structure, Function & Plasticity 3 rd Ed. Enoka Neuromechanics of Human Movement 3 rd Ed. Advantages of spinal stimulation More natural recruitment order of motor units (Mushahwar & Horsch, 2000) Smooth grading of force Fatigue-resistant contractions Elicit functional muscle synergies or reflex circuits from single stimulating electrodes, reducing number of electrodes & controllers (Mushahwar et al. 2002) Mushahwar et al., J Neural Eng 2007 (c) Chet Moritz

14 Cervical spinal stimulation evokes hand & arm movements Perlmutter et al Sunshine, Cho, Lockwood, Fechko, Kasten & Moritz, Journal of Neural Engineering 2013 Cervical ISMS Evoked Movements Elbow Extension Wrist Flexion Sunshine, Cho, Lockwood, Fechko, Kasten & Moritz, Journal of Neural Engineering 2013 (c) Chet Moritz

Collaboration with Josh Smith & Adrienne Fairhall Brain cell activity

15 Brain-Controlled Spinal Interface (BCSI) Brain recording Decode Intention to move Stroke or spinal cord injury Restore muscle function Spinal stimulation Collaboration with Josh Smith & Adrienne Fairhall Brain cell activity correlates with reaching movement Ievins & Moritz, In progress (c) Chet Moritz

16 BCSI restores function after injury Ievins & Moritz, In progress Restoration of function with BCSI Stimulator OFF Stimulator ON Ievins & Moritz, In progress (c) Chet Moritz

Brain-Controlled Spinal Interface (BCSI) Brain recording CMOS implant Skin Wireless Power

injury Spinal injury Spinal stimulation Restore muscle function Generalized linear models

function after SCI or stroke 1. Brain Controlled Interfaces (BCI) for Muscle Stimulation 3.

17 Brain-Controlled Spinal Interface (BCSI) Brain recording CMOS implant Skin Wireless Power Decode intent via implanted computer Wireless data and power link Repair circuits around injury Spinal injury Spinal stimulation Restore muscle function Generalized linear models Collaboration with Josh Smith & Adrienne Fairhall Three approaches to restore limb function after SCI or stroke 1. Brain Controlled Interfaces (BCI) for Muscle Stimulation 3. Spinal Stimulation for Rehabilitation 2. Spinal Stimulation for Re-animation (c) Chet Moritz

Paired Associative Stimulation (PAS) Spike timing dependent

Brain 2000, J Physiol 2002 Jayaram & Steiner Exp Brain Res 2008

leads to stronger connections (via Hebbian plasticity)

18 Paired Associative Stimulation (PAS) Spike timing dependent plasticity Cells that fire together wire together Stefan et al. Brain 2000, J Physiol 2002 Jayaram & Steiner Exp Brain Res 2008 Stimulation induced plasticity Synchronizing cortical sites leads to stronger connections (via Hebbian plasticity) Strengthened connections Jackson et al., Nature 2006 (c) Chet Moritz

Corticospinal plasticity in the intact CNS

stimulation & improves function McPherson,

19 Corticospinal plasticity in the intact CNS Nishimura et al Fetz Neuron 2013 EMG activity dependent spinal stimulation Residual forelimb EMG triggers spinal stimulation & improves function McPherson, Robinson & Perlmutter, PNAS 2015 (c) Chet Moritz

Therapeutic intraspinal microstimulation (ISMS)

Kasten, Sunshine, Secrist, Horner & Moritz, Journal of

after TBI Activity-dependent stimulation (ADS) speeds

20 Therapeutic intraspinal microstimulation (ISMS) promotes recovery beyond the period of stimulation Kasten, Sunshine, Secrist, Horner & Moritz, Journal of Neural Engineering 2013 Cortico-cortico stimulation after TBI Activity-dependent stimulation (ADS) speeds recovery after TBI Guggenmos et al Nudo. PNAS 2013 (c) Chet Moritz

Summary: Neural interfaces for stroke 1. Monkeys can use arbitrary neurons in either hemisphere to control a BCI and muscle stimulation.

Spinal stimulation evokes robust hand & arm synergies in response to brain activity. Is spinal stimulation the ideal output for a brain-computer interface? 3.

Eberhard Fetz Alik Widge Charlie Matlack Rob Robinson Ivana Milovanovic Amber Fechko Larry Shupe Comron Ganji Danielle Lockwood Frances Cho Tia Secasiu Amanda

Aiva Ievins Jaideep Maroovi Eric Secrist Alice Bosma-Moody James Fawcett Rajesh Rao Sarah Mondello Dan Landeck Anat Lubetzky-Vilnai Elena Donoso Brown Torey

21 Summary: Neural interfaces for stroke 1. Monkeys can use arbitrary neurons in either hemisphere to control a BCI and muscle stimulation. Could humans use alternative brain areas for re-animation following stroke? Katie Ris-Vicari 2. Spinal stimulation evokes robust hand & arm synergies in response to brain activity. Is spinal stimulation the ideal output for a brain-computer interface? 3. Spinal stimulation enhances recovery after injury. Can neural interfaces interact with the central nervous system to promote recovery? Eberhard Fetz Alik Widge Charlie Matlack Rob Robinson Ivana Milovanovic Amber Fechko Larry Shupe Comron Ganji Danielle Lockwood Frances Cho Tia Secasiu Amanda Fischedick Cooper Mellema Oliver Stanley Lily Orith-Smith Support Acknowledgements Josh Smith Bing Brunton Phil Horner Steve Perlmutter Mike Kasten Michael Sunshine Aiva Ievins Jaideep Maroovi Eric Secrist Alice Bosma-Moody James Fawcett Rajesh Rao Sarah Mondello Dan Landeck Anat Lubetzky-Vilnai Elena Donoso Brown Torey Gilbertson Tim Morrison Robert Price Reni Magbagbeola Greg Horwitz Nick Donaldson Adrienne Fairhall Howard Chizeck Tom Richner Dianne Rios Anna Pendleton David Bjanes Howard Chizeck Visvesh Sathe Chris Rudell Behnum Habibi Eliza Baird-Daniel Jan Jimenez Grad Students, Postdocs, Undergraduates (c) Chet Moritz

Brain-Computer Interfaces to Replace or Repair the Injured Central Nervous System

Three approaches to restore movement Brain-Computer Interfaces to Replace or Repair the Injured Central Nervous System 1. Replace: Brain control of 2. Replace & Repair: Intra-Spinal Stimulation 3. Repair: